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The effects of bone marrow or periosteum on tendon-to-bone tunnel healing in a rabbit model

  • Knee
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Knee Surgery, Sports Traumatology, Arthroscopy Aims and scope

Abstract

The purpose of this study was to investigate whether a grafting technique using either periosteum or bone marrow as an adjunct, would reconstitute more favorable tendon anchorage morphology with improved tensile strength in a bone tunnel model. We hypothesized that autogenous bone marrow aspirate can enhance the tendon–bone attachment as well as a freshly harvested periosteum, because both tissues contain pluripotent cells. Thirty-six skeletally mature New Zealand white rabbits were utilized. For the tendon graft healing in a bone tunnel model, the extensor digitorum longus tendon was detached from its femoral insertion and transplanted through a bone tunnel into the proximal tibia. Three groups were compared. For the group P (periosteum), a periosteum-wrapped tendon was fixed into the tunnel through the proximal tibial metaphysis. For the group BM (bone marrow), instead of periosteum augmentation, fresh bone marrow was injected into the tendon graft that would sit inside the tunnel. For the group C (control), the limb underwent a similar operation with neither the periosteum enveloping nor bone marrow injecting the tendon. At 6 and 12 weeks after surgery, two rabbits were used for light and electron microscopic examinations, and ten rabbits were used for biomechanical tests in each group. The interface tissue between bone and tendon was thicker and less organized in group C compared to groups P and BM at 6 weeks. Ultra-structurally, the interface tissue was loosely organized in group C, compared to others. Bone ingrowth into tendon was more obvious in groups P and BM, compared to group C. The proliferation of cartilage islands was observed within bone tunnels of both groups P and BM; but a well-defined fibrocartilage zone was noted only in group BM at the interface at week 12. Biomechanical findings: (1) at 6 weeks, the average failure load of group P was significantly higher than the others (P < 0.01). At same time point, in terms of stiffness, while group P was significantly higher than the other groups (P < 0.01), group BM was also significantly higher than that of group C (P < 0.05); (2) at 12 weeks, in terms of failure loads, there was a statistical significant difference only between groups BM and C (P < 0.05). At the same time point, stiffness values were not statistically different among the three groups. Based on the histological and biomechanical findings, the present study demonstrated that periosteum had a positive effect when compared to bone marrow and control groups on the tendon-to-bone healing at an early time point (6 weeks), and bone marrow was also effective at 12 weeks time point compared to the control group in an extra-articular bone tunnel in rabbits. The presence of pluripotent cells in both the bone marrow and the periosteum may be the possible mechanism for enhanced healing. Periosteum had a positive effect at an early time point (6 weeks). Bone marrow was more effective at 12 weeks. Therefore, it is possible that a combination of wrapping periosteum and injecting bone marrow to the tendon graft would have a synergistic effect (early and strong). To prove this hypothesis, future studies which would combine both methods are needed.

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References

  1. Anderson K, Seneviratne AM, Izawa K, Atkinson BL, Potter HG, Rodeo SA (2001) Augmentation of tendon healing in an intraarticular bone tunnel with use of a bone growth factor. Am J Sports Med 29:689–698

    PubMed  CAS  Google Scholar 

  2. Caplan AI (2005) Review: mesenchymal stem cells: cell-based reconstructive therapy in orthopedics. Tissue Eng 11:1198–1211

    Article  PubMed  CAS  Google Scholar 

  3. Chen CH, Chen WJ, Shih CH, Chou SW (2004) Arthroscopic anterior cruciate ligament reconstruction with periosteum-enveloping hamstring tendon graft. Knee Surg Sports Traumatol Arthrosc 12:398–405

    PubMed  Google Scholar 

  4. Chen CH, Chen WJ, Shih CH, Yang CY, Liu SJ, Lin PY (2003) Enveloping the tendon graft with periosteum to enhance tendon–bone healing in a bone tunnel: a biomechanical and histologic study in rabbits. Arthroscopy 19:290–296

    PubMed  Google Scholar 

  5. Cooper RR, Misol S (1970) Tendon and ligament insertion. A light and electron microscopic study. J Bone Joint Surg Am 52:1–20

    PubMed  CAS  Google Scholar 

  6. Goradia VK, Rochat MC, Grana WA, Rohrer MD, Prasad HS (2000) Tendon-to-bone healing of a semitendinosus tendon autograft used for ACL reconstruction in a sheep model. Am J Knee Surg 13:143–151

    PubMed  CAS  Google Scholar 

  7. Hall FL, Han B, Kundu RK, Yee A, Nimni ME, Gordon EM (2001) Phenotypic differentiation of TGF-beta1-responsive pluripotent premesenchymal prehematopoietic progenitor (P4 stem) cells from murine bone marrow. J Hematother Stem Cell Res 10:261–271

    Article  PubMed  CAS  Google Scholar 

  8. Inoue N, Ikeda K, Aro HT, Frassica FJ, Sim FH, Chao EY (2002) Biologic tendon fixation to metallic implant augmented with autogenous cancellous bone graft and bone marrow in a canine model. J Orthop Res 20:957–966

    Article  PubMed  Google Scholar 

  9. Kannus P, Jarvinen M (1987) Conservatively treated tears of the anterior cruciate ligament. Long-term results. J Bone Joint Surg Am 69:1007–1012

    PubMed  CAS  Google Scholar 

  10. Kartus J, Movin T, Karlsson J (2001) Donor-site morbidity and anterior knee problems after anterior cruciate ligament reconstruction using autografts. Arthroscopy 17:971–980

    PubMed  CAS  Google Scholar 

  11. Kyung HS, Kim SY, Oh CW, Kim SJ (2003) Tendon-to-bone tunnel healing in a rabbit model: the effect of periosteum augmentation at the tendon-to-bone interface. Knee Surg Sports Traumatol Arthrosc 11:9–15

    PubMed  Google Scholar 

  12. Lim JK, Hui J, Li L, Thambyah A, Goh J, Lee EH (2004) Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction. Arthroscopy 20:899–910

    PubMed  Google Scholar 

  13. Liu SH, Panossian V, al-Shaikh R, Tomin E, Shepherd E, Finerman GA et al (1997) Morphology and matrix composition during early tendon to bone healing. Clin Orthop Relat Res:253–260

  14. Martinek V, Latterman C, Usas A, Abramowitch S, Woo SL, Fu FH et al (2002) Enhancement of tendon–bone integration of anterior cruciate ligament grafts with bone morphogenetic protein-2 gene transfer: a histological and biomechanical study. J Bone Joint Surg Am 84-A:1123–1131

    PubMed  Google Scholar 

  15. Ohtera K, Yamada Y, Aoki M, Sasaki T, Yamakoshi K (2000) Effects of periosteum wrapped around tendon in a bone tunnel: a biomechanical and histological study in rabbits. Crit Rev Biomed Eng 28:115–118

    PubMed  CAS  Google Scholar 

  16. Ouyang HW, Goh JC, Lee EH (2004) Use of bone marrow stromal cells for tendon graft-to-bone healing: histological and immunohistochemical studies in a rabbit model. Am J Sports Med 32:321–327

    Article  PubMed  Google Scholar 

  17. Park MJ, Lee MC, Seong SC (2001) A comparative study of the healing of tendon autograft and tendon–bone autograft using patellar tendon in rabbits. Int Orthop 25:35–39

    Article  PubMed  CAS  Google Scholar 

  18. Poulsom R, Alison MR, Forbes SJ, Wright NA (2002) Adult stem cell plasticity. J Pathol 197:441–456

    Article  PubMed  Google Scholar 

  19. Ritsila VA, Santavirta S, Alhopuro S, Poussa M, Jaroma H, Rubak JM et al (1994) Periosteal and perichondral grafting in reconstructive surgery. Clin Orthop Relat Res:259–265

  20. Rodeo SA, Arnoczky SP, Torzilli PA, Hidaka C, Warren RF (1993) Tendon-healing in a bone tunnel. A biomechanical and histological study in the dog. J Bone Joint Surg Am 75:1795–1803

    PubMed  CAS  Google Scholar 

  21. Rodeo SA, Suzuki K, Deng XH, Wozney J, Warren RF (1999) Use of recombinant human bone morphogenetic protein-2 to enhance tendon healing in a bone tunnel. Am J Sports Med 27:476–488

    PubMed  CAS  Google Scholar 

  22. Rubak JM (1983) Osteochondrogenesis of free periosteal grafts in the rabbit iliac crest. Acta Orthop Scand 54:826–831

    PubMed  CAS  Google Scholar 

  23. Schmidmaier G, Herrmann S, Green J, Weber T, Scharfenberger A, Haas NP et al (2006) Quantitative assessment of growth factors in reaming aspirate, iliac crest, and platelet preparation. Bone 39:1156–1163

    Article  PubMed  CAS  Google Scholar 

  24. Schneider H (1956) Structure of tendon attachments. Z Anat Entwicklungsgesch 119:431–456

    Article  PubMed  CAS  Google Scholar 

  25. Soon MY, Hassan A, Hui JH, Goh JC, Lee EH (2007) An analysis of soft tissue allograft anterior cruciate ligament reconstruction in a rabbit model: a short-term study of the use of mesenchymal stem cells to enhance tendon osteointegration. Am J Sports Med 35:962–971

    Article  PubMed  Google Scholar 

  26. Wakitani S, Goto T, Pineda SJ, Young RG, Mansour JM, Caplan AI et al (1994) Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 76:579–592

    PubMed  CAS  Google Scholar 

  27. Weiler A, Hoffmann RF, Bail HJ, Rehm O, Sudkamp NP (2002) Tendon healing in a bone tunnel. Part II: Histologic analysis after biodegradable interference fit fixation in a model of anterior cruciate ligament reconstruction in sheep. Arthroscopy 18:124–135

    Article  PubMed  Google Scholar 

  28. Weiler A, Scheffler S, Apreleva M (2006) Healing of ligament and tendon to bone. In: Walsh WR (ed) Repair and regeneration of ligaments, tendons, and joint capsule. Humana Press Inc., Totowa, pp 201–231

    Google Scholar 

  29. Weiss JA, Woo SL, Ohland KJ, Horibe S, Newton PO (1991) Evaluation of a new injury model to study medial collateral ligament healing: primary repair versus nonoperative treatment. J Orthop Res 9:516–528

    Article  PubMed  CAS  Google Scholar 

  30. Yamakado K, Kitaoka K, Yamada H, Hashiba K, Nakamura R, Tomita K (2002) The influence of mechanical stress on graft healing in a bone tunnel. Arthroscopy 18:82–90

    PubMed  Google Scholar 

  31. Youn I, Jones DG, Andrews PJ, Cook MP, Suh JK (2004) Periosteal augmentation of a tendon graft improves tendon healing in the bone tunnel. Clin Orthop Relat Res:223–231

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Acknowledgments

The financial support of Erciyes University Scientific Research Foundation is gratefully acknowledged. The authors thank Esin Asan from Hacettepe University for electonmicroscopic assessment and Mehmet Tuncel MD, Mahmut Argun, MD, and Murat Zumrut, MD, from Erciyes University for their assistance.

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Correspondence to Sinan Karaoglu.

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Karaoglu, S., Celik, C. & Korkusuz, P. The effects of bone marrow or periosteum on tendon-to-bone tunnel healing in a rabbit model. Knee Surg Sports Traumatol Arthrosc 17, 170–178 (2009). https://doi.org/10.1007/s00167-008-0646-3

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  • DOI: https://doi.org/10.1007/s00167-008-0646-3

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